Receptor-Defined Subtypes of Breast Cancer in Indigenous Populations in Africa: A Systematic Review and Meta-Analysis
Background:
Breast cancer is the most common female cancer in Africa. Receptor-defined subtypes are a major determinant of treatment options and disease outcomes but there is considerable uncertainty regarding the frequency of poor prognosis estrogen receptor (ER) negative subtypes in Africa. We systematically reviewed publications reporting on the frequency of breast cancer receptor-defined subtypes in indigenous populations in Africa.
Methods and Findings:
Medline, Embase, and Global Health were searched for studies published between 1st January 1980 and 15th April 2014. Reported proportions of ER positive (ER+), progesterone receptor positive (PR+), and human epidermal growth factor receptor-2 positive (HER2+) disease were extracted and 95% CI calculated. Random effects meta-analyses were used to pool estimates. Fifty-four studies from North Africa (n = 12,284 women with breast cancer) and 26 from sub-Saharan Africa (n = 4,737) were eligible. There was marked between-study heterogeneity in the ER+ estimates in both regions (I2>90%), with the majority reporting proportions between 0.40 and 0.80 in North Africa and between 0.20 and 0.70 in sub-Saharan Africa. Similarly, large between-study heterogeneity was observed for PR+ and HER2+ estimates (I2>80%, in all instances). Meta-regression analyses showed that the proportion of ER+ disease was 10% (4%–17%) lower for studies based on archived tumor blocks rather than prospectively collected specimens, and 9% (2%–17%) lower for those with ≥40% versus those with <40% grade 3 tumors. For prospectively collected samples, the pooled proportions for ER+ and triple negative tumors were 0.59 (0.56–0.62) and 0.21 (0.17–0.25), respectively, regardless of region. Limitations of the study include the lack of standardized procedures across the various studies; the low methodological quality of many studies in terms of the representativeness of their case series and the quality of the procedures for collection, fixation, and receptor testing; and the possibility that women with breast cancer may have contributed to more than one study.
Conclusions:
The published data from the more appropriate prospectively measured specimens are consistent with the majority of breast cancers in Africa being ER+. As no single subtype dominates in the continent availability of receptor testing should be a priority, especially for young women with early stage disease where appropriate receptor-specific treatment modalities offer the greatest potential for reducing years of life lost.
Please see later in the article for the Editors' Summary
Vyšlo v časopise:
Receptor-Defined Subtypes of Breast Cancer in Indigenous Populations in Africa: A Systematic Review and Meta-Analysis. PLoS Med 11(9): e32767. doi:10.1371/journal.pmed.1001720
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pmed.1001720
Souhrn
Background:
Breast cancer is the most common female cancer in Africa. Receptor-defined subtypes are a major determinant of treatment options and disease outcomes but there is considerable uncertainty regarding the frequency of poor prognosis estrogen receptor (ER) negative subtypes in Africa. We systematically reviewed publications reporting on the frequency of breast cancer receptor-defined subtypes in indigenous populations in Africa.
Methods and Findings:
Medline, Embase, and Global Health were searched for studies published between 1st January 1980 and 15th April 2014. Reported proportions of ER positive (ER+), progesterone receptor positive (PR+), and human epidermal growth factor receptor-2 positive (HER2+) disease were extracted and 95% CI calculated. Random effects meta-analyses were used to pool estimates. Fifty-four studies from North Africa (n = 12,284 women with breast cancer) and 26 from sub-Saharan Africa (n = 4,737) were eligible. There was marked between-study heterogeneity in the ER+ estimates in both regions (I2>90%), with the majority reporting proportions between 0.40 and 0.80 in North Africa and between 0.20 and 0.70 in sub-Saharan Africa. Similarly, large between-study heterogeneity was observed for PR+ and HER2+ estimates (I2>80%, in all instances). Meta-regression analyses showed that the proportion of ER+ disease was 10% (4%–17%) lower for studies based on archived tumor blocks rather than prospectively collected specimens, and 9% (2%–17%) lower for those with ≥40% versus those with <40% grade 3 tumors. For prospectively collected samples, the pooled proportions for ER+ and triple negative tumors were 0.59 (0.56–0.62) and 0.21 (0.17–0.25), respectively, regardless of region. Limitations of the study include the lack of standardized procedures across the various studies; the low methodological quality of many studies in terms of the representativeness of their case series and the quality of the procedures for collection, fixation, and receptor testing; and the possibility that women with breast cancer may have contributed to more than one study.
Conclusions:
The published data from the more appropriate prospectively measured specimens are consistent with the majority of breast cancers in Africa being ER+. As no single subtype dominates in the continent availability of receptor testing should be a priority, especially for young women with early stage disease where appropriate receptor-specific treatment modalities offer the greatest potential for reducing years of life lost.
Please see later in the article for the Editors' Summary
Zdroje
1. International Agency for Research on Cancer (2012) GLOBOCAN 2012. Available: http://globocaniarcfr/. Accessed 17 April 2014.
2. YangXR, Chang-ClaudeJ, GoodeEL, CouchFJ, NevanlinnaH, et al. (2011) Associations of breast cancer risk factors with tumor subtypes: a pooled analysis from the Breast Cancer Association Consortium studies. J Natl Cancer Inst 103: 250–263.
3. BlowsFM, DriverKE, SchmidtMK, BroeksA, van LeeuwenFE, et al. (2010) Subtyping of breast cancer by immunohistochemistry to investigate a relationship between subtype and short and long term survival: a collaborative analysis of data for 10,159 cases from 12 studies. PLoS Med 7: e1000279.
4. DaviesC, GodwinJ, GrayR, ClarkeM, CutterD, et al. (2011) Relevance of breast cancer hormone receptors and other factors to the efficacy of adjuvant tamoxifen: patient-level meta-analysis of randomised trials. Lancet 378: 771–784.
5. JemalA, FedewaSA (2012) Is the prevalence of ER-negative breast cancer in the US higher among Africa-born than US-born black women? Breast Cancer Res Treat 135: 867–873.
6. Surveillance Epidemiology and End Results (SEER) Program (Available: www.seer.cancer.gov) SEER*Stat Database: Incidence, SEER 17 Regs Research Data+Hurricane Katrina Impacted Louisiana Cases, Nov 2010 Sub (1973–2008 varying), Linked To County Attributes. 2010. Total U.S., 1969–2009 Counties, National Cancer Institute, DCCPS, Surveillance Research Program, Cancer Statistics Branch released April 2011 (updated 10/28/2011). Ref Type: Report
7. BirdPA, HillAG, HoussamiN (2008) Poor hormone receptor expression in East African breast cancer: evidence of a biologically different disease? Ann Surg Oncol 15: 1983–1988.
8. HuoD, IkpattF, KhramtsovA, DangouJM, NandaR, et al. (2009) Population differences in breast cancer: Survey in indigenous african women reveals over-representation of triple-negative breast cancer. J Clin Oncology 27: 4515–4521.
9. McCormackVA, JoffeM, van den BergE, BroezeN, dos Santos SilvaI, et al. (2013) Breast cancer receptor status and stage at diagnosis in over 1,200 consecutive public hospital patients in Soweto, South Africa: a case series. Breast Cancer Res 15: R84.
10. AdebamowoCA, FamootoA, OgundiranTO, AniagwuT, NkwodimmahC, et al. (2008) Immunohistochemical and molecular subtypes of breast cancer in Nigeria. Breast Cancer Res Treat 110: 183–188.
11. KriegerN, ChenJT, WatermanPD (2011) Temporal trends in the black/white breast cancer case ratio for estrogen receptor status: disparities are historically contingent, not innate. Cancer Causes Control 22: 511–514.
12. Global Health (2014) Available: http://www.cabi.org/publishing-products/online-information-resources/global-health/.
13. LodgeM, CorbexM (2011) Establishing an evidence-base for breast cancer control in developing countries. Breast 20 Suppl 2S65–69.
14. The Cochrane Collaboration Cochrane Handbook for Systematic Reviews of Interventions 2009. Available: http://handbook.cochrane.org/
15. United Nations (2013) United Nations Composition of macro geographical (continental) regions, geographical sub-regions, and selected economic and other groupings. Available: http://unstats.un.org/unsd/methods/m49/m49regin.htm. Accessed 10 December 2013.
16. HigginsJ, ThompsonS (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21: 1539–1558.
17. HigginsJP, ThompsonSG, DeeksJJ, AltmanDG (2003) Measuring inconsistency in meta-analyses. BMJ 327: 557–560.
18. EggerM, Davey SmithG, SchneiderM, MinderC (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315: 629–634.
19. McCarthyNJ, YangX, LinnoilaIR, MerinoMJ, HewittSM, et al. (2002) Microvessel density, expression of estrogen receptor alpha, MIB-1, p53, and c-erbB-2 in inflammatory breast cancer. Clin Cancer Res 8: 3857–3862.
20. ElgailiEM, AbuidrisDO, RahmanM, MichalekAM, MohammedSI (2010) Breast cancer burden in central Sudan. Int J Womens Health 2: 77–82.
21. Ben GacemR, HachanaM, ZiadiS, Ben AbdelkarimS, HidarS, et al. (2012) Clinicopathologic significance of DNA methyltransferase 1, 3a, and 3b overexpression in Tunisian breast cancers. Hum Pathol 43: 1731–1738.
22. SnoussiK, MahfoudhW, BouaouinaN, FekihM, KhairiH, et al. (2010) Combined effects of IL-8 and CXCR2 gene polymorphisms on breast cancer susceptibility and aggressiveness. BMC Cancer 10: 283.
23. HamritaB, Ben NasrH, GabboujS, BouaouinaN, ChouchaneL, et al. (2011) Apolipoprotein A1 −75 G/A and +83 C/T polymorphisms: susceptibility and prognostic implications in breast cancer. Mol Biol Rep 38: 1637–1643.
24. HachanaM, TrimecheM, ZiadiS, AmaraK, GaddasN, et al. (2008) Prevalence and characteristics of the MMTV-like associated breast carcinomas in Tunisia. Cancer Lett 271: 222–230.
25. Ali-LabibR, El-MonemF (2009) Hypermethylation of the tumour suppressor RassF1A gene in malignant and benign breast tissues from Egyptian patients. The Egyptian Journal of Biochemistry & Molecular Biology 27: 83–100.
26. BoufettalH, NounM, SamouhN (2010) [Breast cancer in young patient in Morocco]. Cancer Radiother 14: 698–703.
27. MarrakchiR, KhadimallahI, OuerhaniS, GamoudiA, KhomsiF, et al. (2010) Expression of WISP3 and RhoC genes at mRNA and protein levels in inflammatory and noninflammatory breast Cancer in Tunisian patients. Cancer Invest 28: 399–407.
28. Ben HamidaA, LabidiIS, MradK, Charafe-JauffretE, Ben ArabS, et al. (2008) Markers of subtypes in inflammatory breast cancer studied by immunohistochemistry: prominent expression of P-cadherin. BMC Cancer 8: 28.
29. AbbasH, SalemAAS, SalemMAE, BinziadS, GamalB (2011) Breast cancer: radiotherapy at the South Egypt Cancer Institute. Gastric and Breast Cancer 10: 180–186.
30. LeMG, ArriagadaR, ContessoG, CammounM, PfeifferF, et al. (2005) Dermal lymphatic emboli in inflammatory and noninflammatory breast cancer: A French-Tunisian joint study in 337 partients. Clin Breast Cancer 6: 439–445.
31. HusseinYM, GharibAF, EtewaRL, El-ShalAS, Abdel-GhanyME, et al. (2011) The melanoma-associated antigen-A3, -A4 genes: relation to the risk and clinicopathological parameters in breast cancer patients. Mol Cell Biochem 351: 261–268.
32. Karray-ChouayekhS, TrifaF, KhabirA, BoujelbeneN, Sellami-BoudawaraT, et al. (2011) Methylation status and overexpression of COX-2 in Tunisian patients with ductal invasive breast carcinoma. Tumour Biol 32: 461–468.
33. El-HawaryAK, AbbasAS, ElsayedAA, ZalataKR (2012) Molecular subtypes of breast carcinoma in Egyptian women: clinicopathological features. Pathol Res Pract 208: 382–386.
34. BennisS, AbbassF, AkasbiY, ZnatiK, JouteiKA, et al. (2012) Prevalence of molecular subtypes and prognosis of invasive breast cancer in north-east of Morocco: retrospective study. BMC Research Notes 5: 436.
35. MarrakchiR, OuerhaniS, BenammarS, RouissiK, BouhahaR, et al. (2008) Detection of cytokeratin 19 mRNA and CYFRA 21-1 (cytokeratin 19 fragments) in blood of Tunisian women with breast cancer. Int J Biol Markers 23: 238–243.
36. BaccoucheS, DaoudJ, FrikhaM, Mokdad-GargouriR, GargouriA, et al. (2003) Immunohistochemical Status of p53, MDM2, bcl2, bax, and ER in Invasive Ductal Breast Carcinoma in Tunisian Patients. Ann N Y Acad Sci 1010: 752–763.
37. MaalejM, HentatiD, MessaiT, KochbatiL, El MayA, et al. (2008) Breast cancer in Tunisia in 2004: a comparative clinical and epidemiological study. Bull Cancer 95: E5–9.
38. El-RehimD, AliM (2009) Aberrant expression of beta-catenin in invasive ductal breast carcinomas. Journal of the Egyptian National Cancer Institute 21: 185–195.
39. AyadiL, KhabirA, AmouriH, KarrayS, DammakA, et al. (2008) Correlation of HER-2 over-expression with clinico-pathological parameters in Tunisian breast carcinoma. World J Surg Oncol 6: 112.
40. MohammadAM, AbdelHA, AbdelW, AhmedAM, WaelT, et al. (2006) Expression of cyclooxygenase-2 and 12-lipoxygenase in human breast cancer and their relationship with HER-2/neu and hormonal receptors: impact on prognosis and therapy. Indian J Cancer 43: 163–168.
41. Karray-ChouayekhS, TrifaF, KhabirA, BoujelbaneN, Sellami-BoudawaraT, et al. (2010) Aberrant methylation of RASSF1A is associated with poor survival in Tunisian breast cancer patients. J Cancer Res Clin Oncol 136: 203–210.
42. MoonaMS, AlarabiRAR, HussainA, AhmadM, MehdiI (2010) The study of ER (Oestrogen Receptor), PR (Progesterone Receptor) and HER-2/neu status in patients with breast cancer. Jamahiriya Medical Journal 10: 141–143.
43. ZeeneldinAA, MohamedAM, AbdelHA, TahaFM, GodaIA, et al. (2009) Survival effects of cyclooxygenase-2 and 12-lipooxygenase in Egyptian women with operable breast cancer. Indian J Cancer 46: 54–60.
44. TazziteA, JouhadiH, SaissK, BeniderA, NadifiS (2013) Relationship between family history of breast cancer and clinicopathological features in moroccan patients. Ethiop J Health Sci 23: 150–157.
45. RashedMM, RagabNM, GalalMK (2007) The association of HER-2/neu over-expression in relation to p53 nuclear accumulation, hormonal recceptor status and common clinico-pathological prognostic parameters in a series of Egyptian women with invasive ductal carcinoma. European Journal of General Medicine 4: 73–79.
46. LoueslatiBY, TroudiW, CherniL, RhomdhaneKB, Mota-VieiraL (2010) Germline HVR-II mitochondrial polymorphisms associated with breast cancer in Tunisian women. Genet Mol Res 9: 1690–1700.
47. AbdelkrimSB, TrabelsiA, MissaouiN, BeizigN, BdiouiA, et al. (2010) Distribution of molecular breast cancer subtypes among Tunisian women and correlation with histopathological parameters: A study of 194 patients. Pathol Res Pract 206: 772–775.
48. AwadelkarimKD, ArizziC, ElaminEOM, HamadHMA, BlasioPd, et al. (2008) Pathological, clinical and prognostic characteristics of breast cancer in Central Sudan versus Northern Italy: implications for breast cancer in Africa. Histopathology 52: 445–456.
49. SalhiaB, TapiaC, IshakEA, GaberS, BerghuisB, et al. (2011) Molecular subtype analysis determines the association of advanced breast cancer in Egypt with favorable biology. BMC Womens Health 11.
50. El MongyM, El HossienyH, HaggagF, FathyR (2010) Clinico-pathological study and treatment results of 1009 operable breast cancer cases: Experience of NCI Cairo University, Egypt. Chinese-German Journal of Clinical Oncology 9: 409–415.
51. Abu-BedairFA, El-GamalBA, IbrahimNA, El-AaserAA (2000) Hormonal profiles and estrogen receptors in Egyptian female breast cancer patients. Tumori 86: 24–29.
52. HusseinO, MosbahM, FaroukO, FaragK, El-SaedA, et al. (2013) Hormone receptors and age distribution in breast cancer patients at a university hospital in northern Egypt. Breast Cancer: Basic and Clinical Research 7: 51–57.
53. KallelI, KharratN, Al-fadhlyS, RebaiM, KhabirA, et al. (2010) HER2 polymorphisms and breast cancer in Tunisian women. Genet Test Mol Biomarkers 14: 29–35.
54. MarzoukD, GaafaryM, DamatyS, SabbourS, MeckyF, et al. (2009) Breast cancer and hormonal intake among Egyptian females. Eur J Oncol 14: 37–51.
55. ChaherN, Arias-PulidoH, TerkiN, QuallsC, BouzidK, et al. (2012) Molecular and epidemiological characteristics of inflammatory breast cancer in Algerian patients. Breast Cancer Res Tr 131: 437–444.
56. YoussefN, HewediI, RabohN (2008) Immunohistochemical expression of survivin in breast carcinoma: relationship with clinicopathological parameters, proliferation and molecular classification. Journal of the Egyptian National Cancer Institute 20: 348–357.
57. ErmiahE, BuhmeidaA, KhaledBR, AbdallaF, SalemN, et al. (2013) Prognostic value of bcl-2 expression among women with breast cancer in Libya. Tumour Biol 34: 1569–1578.
58. AsaadNY, KandilMAEH, ShabanMI (2003) Prognostic significance of maspin expression in breast carcinoma. Cancer Mol Biol 10: 1937–1951.
59. HafezN, TahounN (2010) Assessment of the reliability of immunocytochemical detection of estrogen and progesterone receptors status on the cytological aspiarates of breast carcinoma. Journal of the Egyptian National Cancer Institute 22: 217–225.
60. SwellamM, IsmailM, EissaS, HamdyM, MokhtarN (2004) Emerging role of P53, Bcl-2 and telomerase activity in Egyptian breast cancer patients. IUBMB Life 56: 483–490.
61. Abdel-FattahM, LotfyNS, BassiliA, AnwarM, MariE, et al. (2001) Current treatment modalities of breast-cancer patients in Alexandria, Egypt. Breast 10: 523–529.
62. AlieldinNH, Abo-ElazmOM, BilalD, SalemSE, GoudaE, et al. (2014) Age at diagnosis in women with non-metastatic breast cancer: Is it related to prognosis? Journal of the Egyptian National Cancer Institute 26: 23–30.
63. BoderJ, AbdallaF, ElfagiehM, BuhmeidaA, CollanY (2013) Proliferative activity in Libyan breast cancer with comparison to European and central African patients. BioMed Research International 2013.
64. BouzidN, LahmarR, TebraS, BouaouinaN (2013) Breast cancer in woman younger than 35 years in Tunisia: Retrospective study about 124 cases. [French] Cancer du sein chez la femme jeune de moins de 35 ans en Tunisie: etude retrospective a propos de 124 cas. Gynecologie Obstetrique Fertilite 41: 356–360.
65. ElesawyBH, Abd El HafezA, ShawkyAEA, ArafaM (2014) Immunohistochemistry-based subtyping of breast carcinoma in Egyptian women: a clinicopathologic study on 125 patients. Ann Diagn Pathol 18: 21–26.
66. El-ShinawiM, MohamedHT, El-GhonaimyEA, TantawyM, YounisA, et al. (2013) Human cytomegalovirus infection enhances NF- kappa B/p65 signaling in inflammatory breast cancer patients. PLoS ONE 8: e55755.
67. HagrassHA, PashaHF, ShaheenMA, Abdel BaryEH, KassemR (2014) Methylation status and protein expression of RASSF1A in breast cancer patients. Mol Biol Rep 41: 57–65.
68. IsmailiN, ElyaakoubiH, BensoudaY, ErrihaniH (2014) Demographic, clinical, pathological, molecular, treatment characteristics and outcomes of nonmetastatic inflammatory breast cancer in Morocco: 2007 and 2008. Experimental Hematology and Oncology 3.
69. RashadYA, ElkhodaryTR, El-GayarAM, EissaLA (2014) Evaluation of serum levels of HER2, MMP-9, nitric oxide, and total antioxidant capacity in Egyptian breast cancer patients: correlation with clinico-pathological parameters. Scientia Pharmaceutica 82: 129–145.
70. BekkoucheZ, GuedouarY, Ben AliF, El KebirFZ (2013) Characteristics of triple-negative breast carcinomas in west Algeria. [French] Caracteristiques des carcinomes mammaires triple-negatifs dans l'Ouest-algerien. Journal Africain du Cancer 5: 155–161.
71. SalamaA, El-FendyH, TalaatS, BayomiB, AminA (2013) Prognostic value of immunohistochemical stratification of invasive duct carcinoma of the breast. Chinese-German Journal of Clinical Oncology 12: P265–P272.
72. HirkoKA, SolimanAS, HablasA, SeifeldinIA, RamadanM, et al. (2013) Trends in breast cancer incidence rates by age and stage at diagnosis in gharbiah, Egypt, over 10 years (1999–2008). Journal of Cancer Epidemiology 2013.
73. DeyS, SolimanAS, HablasA, SeifeldinIA, IsmailK, et al. (2010) Urban-rural differences in breast cancer incidence by hormone receptor status across 6 years in Egypt. Breast Cancer Res Treat 120: 149–160.
74. UgiagbeEE, ObasekiDE, OluwasolaAO, Olu-EddoAN, AkhiwuWO (2012) Frequency of distribution of oestrogen and progesterone receptors positivities in breast cancer cases in Benin-City, Nigeria. Nigerian Postgraduate Medical Journal 19: 19–24.
75. IyareF (2007) Immunohistochemical characteristics of breast cancers in South East Nigeria. Ebonyi Medical Journal 6: 9–12.
76. AgboolaAJ, MusaAA, WanangwaN, Abdel-FatahT, NolanCC, et al. (2012) Molecular characteristics and prognostic features of breast cancer in Nigerian compared with UK women. Breast Cancer Res Treat 135: 555–569.
77. IkpattOF, Ndoma-EgbaR (2003) Oestrogen and progesterone receptors in Nigerian breast cancer: relationship to tumour histopathology and survival of patients. Cent Afr J Med 49: 122–126.
78. StarkA, KleerCG, MartinI, AwuahB, Nsiah-AsareA, et al. (2010) African ancestry and higher prevalence of triple-negative breast cancer: findings from an international study. Cancer 116: 4926–4932.
79. GukasID, JenningsBA, MandongBM, IgunGO, GirlingAC, et al. (2005) Clinicopathological features and molecular markers of breast cancer in Jos, Nigeria. West Afr J Med 24: 209–213.
80. SchwartzT, StarkA, PangJ, AwuahB, KleerCG, et al. (2013) Expression of aldehyde dehydrogenase 1 as a marker of mammary stem cells in benign and malignant breast lesions of Ghanaian women. Cancer 119: 488–494.
81. MbondeMP, AmirH, AkslenLA, KitinyaJN (2001) Expression of oestrogen and progesterone receptors, Ki-67, p53 and BCL-2 proteins, cathepsin D, urokinase plasminogen activator and urokinase plasminogen activator-receptors in carcinomas of the female breast in an African population. East Afr Med J 78: 360–365.
82. NyagolJ, Nyong'oA, ByakikaB, MuchiriL, CoccoM, et al. (2006) Routine assessment of hormonal receptor and her-2/neu status underscores the need for more therapeutic targets in Kenyan women with breast cancer. Anal Quant Cytol Histol 28: 97–103.
83. NalwogaH, ArnesJB, WabingaH, AkslenLA (2010) Expression of aldehyde dehydrogenase 1 (ALDH1) is associated with basal-like markers and features of aggressive tumours in African breast cancer. Br J Cancer 102: 369–375.
84. LyM, AntoineM, DembeleAK, LevyP, RodenasA, et al. (2012) High incidence of triple-negative tumors in sub-saharan Africa: a prospective study of breast cancer characteristics and risk factors in Malian women seen in a Bamako university hospital. Oncology 83: 257–263.
85. YarneyJ, VanderpuyeV, Clegg LampteyJN (2008) Hormone receptor and HER-2 expression in breast cancers among Sub-Saharan African women. Breast J 14: 510–511.
86. GalukandeM, WabingaH, MirembeF, KaramagiC, AseaA (2013) Difference in risk factors for breast cancer by ER status in an indigenous African population. ISRN Oncology 1.
87. Ohene-YeboahM, AdjeiE (2012) Breast cancer in Kumasi, Ghana. Ghana Medical Journal 46: 8–13.
88. BursonAM, SolimanAS, NgomaTA, MwaiselageJ, OgweyoP, et al. (2010) Clinical and epidemiologic profile of breast cancer in Tanzania. Breast Dis 31: 33–41.
89. SavageN, LevinJ, De MoorNG, LangeM (1981) Cytosolic oestrogen receptor content of breast cancer tissue in blacks and whites. S Afr Med J 59: 623–624.
90. WintersZ, MannellA, EsserJD (1988) Breast cancer in black South Africans. S Afr J Surg 26: 69–70.
91. CollingsJR, LevinJ, SavageN (1980) Racial differences in oestrogen receptor and peroxidase status of human breast cancer tissue. S Afr Med J 57: 444–446.
92. Van BogaertLJ (2013) Breast cancer molecular subtypes as identified by immunohistochemistry in South African black women. Breast Journal 19: 210–211.
93. BasroS, ApffelstaedtJP (2010) Breast cancer in young women in a limited-resource environment. World J Surg 34: 1427–1433.
94. TogoA, KanteL, DembeleBT, TraoreA, DiakiteI, et al. (2010) Breast cancer in Bamako hospitals: epidemiologic and diagnostic aspects. Medecine d'Afrique Noire 57: 249–253.
95. Emile HasiniatsyNR, VololonantenainaCR, RabarikotoHF, RazafimanjatoN, RanoharisonHD, et al. (2014) First results of hormone receptors' status in Malagasy women with invasive breast cancer. Pan African Medical Journal 17.
96. KhouryT, SaitS, HwangH, ChandrasekharR, WildingG, et al. (2009) Delay to formalin fixation effect on breast biomarkers. Mod Pathol 22: 1457–1467.
97. WasielewskiR, HasselmannS, RuschoffJ, Fisseler-EckhoffA, KreipeH (2008) Proficiency testing of immunohistochemical biomarker assays in breast cancer. Virchows Arch 453: 537–543.
98. HammondME, HayesDF, WolffAC, ManguPB, TeminS (2010) American society of clinical oncology/college of american pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. J Oncol Pract 6: 195–197.
99. MoultrieTA, SayiTS, TimaeusIM (2012) Birth intervals, postponement, and fertility decline in Africa: a new type of transition? Popul Stud (Camb) 66: 241–258.
100. PelletierD, RahnM (1998) Trends in body mass index in developing countries. Food Nutr Bull 19: 223–238.
101. JamesP (2004) Obesity: the worldwide epidemic. Clin Dermatol 22: 276–280.
102. ClarkeC, KeeganT, YangJ, PressD, KurianA, et al. (2012) Age-specific incidence of breast cancer subtypes: understanding the black-white crossover. J Natl Cancer Inst 104: 1094–1101.
103. Vona-DavisL, RoseD, HazardH, Howard-McNattM, AdkinsF, et al. (2008) Triple-negative breast cancer and obesity in a rural Appalachian population. Cancer Epidemiol Biomarkers Prev 17: 3319–3324.
104. PhippsA, ChlebowskiR, PrenticeR, McTiernanA, Wactawski-WendeJ, et al. (2011) Reproductive history and oral contraceptive use in relation to risk of triple-negative breast cancer. J Natl Cancer Inst 103: 470–477.
105. DolleJ, DalingJ, WhiteE, BrintonL, DoodyD, et al. (2009) Risk factors for triple-negative breast cancer in women under the age of 45 years. Cancer Epidemiol Biomarkers Prev 18: 1157–1166.
106. PalmerJ, Ruiz-NarvaezE, RotimiC, CupplesL, CozierY, et al. (2013) Genetic susceptibility loci for subtypes of breast cancer in an African American population. Cancer Epidemiol Biomarkers Prev 22: 127–134.
107. Ruiz-NarvaezE, RosenbergL, RotimiC, CupplesL, BoggsD, et al. (2010) Genetic variants on chromosome 5p12 are associated with risk of breast cancer in African American women: the Black Women's Health Study. Breast Cancer Res Treat 123: 525–530.
108. SuY, ZhengY, ZhengW, GuK, ChenZ, et al. (2011) Distinct distribution and prognostic significance of molecular subtypes of breast cancer in Chinese women: a population-based cohort study. BMC Cancer 11: 292.
109. CareyLA, PerouCM, LivasyCA, DresslerLG, CowanD, et al. (2006) Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA 295: 2492–2502.
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